A urea channel from Bacillus cereus reveals a novel hexameric structure

Biochemical Journal

Volumn 445, Issue 2, 2012, Pages 157-166

  Huysmans, Gerard H M ^a,d   Chan, Nathan ^b   Baldwin, Jocelyn M ^a   Postis, Vincent L G ^a   Tzokov, Svetomir B ^b   Deacon, Sarah E ^a   Yao, Sylvia Y M ^c   Young, James D ^c   McPherson, Michael J ^a   Bullough, Per A ^b   Baldwin, Stephen A ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

^c UNIVERSITY OF ALBERTA   (Canada)

^d INSTITUT PASTEUR   (France)

Author keywords

Cryo electron microscopy; Electron crystallography; Helicobacter pylori; Membrane; Protein structure; Urea channel

Indexed keywords

OLIGOMER; PHOSPHOLIPID; PROTEOLIPOSOME; UREA;

AMINO ACID SEQUENCE; ARTICLE; BACILLUS CEREUS; BIOINFORMATICS; CIRCULAR DICHROISM; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; CRYSTAL; CRYSTALLOGRAPHY; FLUORESCENCE; GEL PERMEATION CHROMATOGRAPHY; HELICOBACTER PYLORI; INFRARED SPECTROSCOPY; MEMBRANE CHANNEL; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; BACILLUS CEREUS; BACTERIAL PROTEINS; CRYOELECTRON MICROSCOPY; ION CHANNELS; MEMBRANE TRANSPORT PROTEINS; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, SECONDARY; SEQUENCE HOMOLOGY, AMINO ACID; UREA;

BACILLUS CEREUS; HELICOBACTER PYLORI;

EID: 84863197430     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20120169     Document Type: Article

References (43)

1. Stewart, G. (2011) The emerging physiological roles of the SLC14A family of urea transporters. Br. J. Pharmacol. 164, 1780-1792
2. Sachs, G., Kraut, J. A., Wen, Y., Feng, J. and Scott, D. R. (2007) Urea transport in bacteria: acid acclimation by gastric Helicobacter spp. J. Membr. Biol. 212, 71-82 (Pubitemid 46292323)
3. + symporter in Aspergillus nidulans. Fungal Genet. Biol. 47, 1023-1033
4. Beckers, G., Bendt, A. K., Kramer, R. and Burkovski, A. (2004) Molecular identification of the urea uptake system and transcriptional analysis of urea transporter- and urease-encoding genes in Corynebacterium glutamicum. J. Bacteriol. 186, 7645-7652 (Pubitemid 39463730)
5. Levin, E. J., Quick, M. and Zhou, M. (2009) Crystal structure of a bacterial homologue of the kidney urea transporter. Nature 462, 757-761
6. Mollenhauer-Rektorschek, M., Hanauer, G., Sachs, G. and Melchers, K. (2002) Expression of UreI is required for intragastric transit and colonization of gerbil gastric mucosa by Helicobacter pylori. Res. Microbiol. 153, 659-666 (Pubitemid 35449269)
7. + -gated urea channel: the link between Helicobacter pylori urease and gastric colonization. Science 287, 482-485
8. Fox, J. G. and Wang, T. C. (2007) Inflammation, atrophy, and gastric cancer. J. Clin. Invest. 117, 60-69 (Pubitemid 46048450)
9. Selgrad, M. and Malfertheiner, P. (2011) Treatment of Helicobacter pylori. Curr. Opin. Gastroenterol. 27, 565-570
10. Gray, L. R., Gu, S. X., Quick, M. and Khademi, S. (2011) Transport kinetics and selectivity of HpUreI, the urea channel from Helicobacter pylori. Biochemistry 50, 8656-8663
11. Ivanova, N., Sorokin, A., Anderson, I., Galleron, N., Candelon, B., Kapatral, V., Bhattacharyya, A., Reznik, G., Mikhailova, N., Lapidus, A. et al. (2003) Genome sequence of Bacillus cereus and comparative analysis with Bacillus anthracis. Nature 423, 87-91 (Pubitemid 36569587)
12. Roach, P. C., Postis, V. L., Deacon, S. E., Wright, G. S., Ingram, J. C., Xia, X., McPherson, M. J. and Baldwin, S. A. (2008) Large-scale preparation of bacterial cell membranes by tangential flow filtration. Mol. Membr. Biol. 25, 609-616
13. Postis, V. L., Deacon, S. E., Roach, P. C., Wright, G. S., Xia, X., Ingram, J. C., Hadden, J. M., Henderson, P. J., Phillips, S. E., McPherson, M. J. and Baldwin, S. A. (2008) A high-throughput assay of membrane protein stability. Mol. Membr. Biol. 25, 617-624
14. Deacon, S. E., Roach, P.C.J., Postis, V.L.G., Wright, G.S.A., Xia, X., Phillips, S.E.V., Knox, J. P., Henderson, P.J.F., McPherson, M. J. and Baldwin, S. A. (2008) Reliable scale-up of membrane protein over-expression by bacterial auto-induction: from microwell plates to pilot scale fermentations. Mol. Membr. Biol. 25, 588-598
15. Goormaghtigh, E., Cabiaux, V. and Ruysschaert, J. M. (1994) Determination of soluble and membrane protein structure by Fourier transform infrared spectroscopy. III. Secondary structures. Subcell. Biochem. 23, 405-450
16. Tatulian, S. A. (2003) Attenuated total reflection Fourier transform infrared spectroscopy: a method of choice for studying membrane proteins and lipids. Biochemistry 42, 11898-11907
17. Goormaghtigh, E., Raussens, V. and Ruysschaert, J. M. (1999) Attenuated total reflection infrared spectroscopy of proteins and lipids in biological membranes. Biochim. Biophys. Acta 1422, 105-185 (Pubitemid 29313327)
18. Slotboom, D. J., Duurkens, R. H., Olieman, K. and Erkens, G. B. (2008) Static light scattering to characterize membrane proteins in detergent solution. Methods 46, 73-82
19. Ye, L., Jia, Z., Jung, T. and Maloney, P. C. (2001) Topology of OxlT, the oxalate transporter of Oxalobacter formigenes, determined by site-directed fluorescence labeling. J. Bacteriol. 183, 2490-2496 (Pubitemid 32249757)
20. Godara, G., Smith, C., Bosse, J., Zeidel, M. and Mathai, J. (2009) Functional characterization of Actinobacillus pleuropneumoniae urea transport protein, ApUT. Am. J. Physiol. Regul. Integr. Comp. Physiol. 296, R1268-R1273
21. Jap, B. K., Zulauf, M., Scheybani, T., Hefti, A., Baumeister, W., Aebi, U. and Engel, A. (1992) 2D crystallization: from art to science. Ultramicroscopy 46, 45-84 (Pubitemid 23600814)
22. Glover, C. A., Postis, V. L., Charalambous, K., Tzokov, S. B., Booth, W. I., Deacon, S. E., Wallace, B. A., Baldwin, S. A. and Bullough, P. A. (2011) AcrB contamination in 2-D crystallization of membrane proteins: lessons from a sodium channel and a putative monovalent cation/proton antiporter. J. Struct. Biol. 176, 419-424
23. Gipson, B., Zeng, X., Zhang, Z. Y. and Stahlberg, H. (2007) 2dx: user-friendly image processing for 2D crystals. J. Struct. Biol. 157, 64-72 (Pubitemid 44880797)
24. Henderson, R., Baldwin, J. M., Downing, K. H., Lepault, J. and Zemlin, F. (1986) Structure of purple membrane from Halobacterium halobium: recording, measurement and evaluation of electron micrographs at 3.5 Å resolution. Ultramicroscopy 19, 147-178
25. Valpuesta, J. M., Carrascosa, J. L. and Henderson, R. (1994) Analysis of electron microscope images and electron diffraction patterns of thin crystals of Φ29 connectors in ice. J. Mol. Biol. 240, 281-287
26. Crowther, R. A., Henderson, R. and Smith, J. M. (1996) MRC image processing programs. J. Struct. Biol. 116, 9-16 (Pubitemid 26093117)
27. Havelka, W. A., Henderson, R. and Oesterhelt, D. (1995) Three-dimensional structure of halorhodopsin at 7 Å resolution. J. Mol. Biol. 247, 726-738
28. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr. Sect. D Biol. Crystallogr. 50, 760-763
29. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. and Higgins, D. G. (1997) The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876-4882 (Pubitemid 28022245)
30. Berezin, C., Glaser, F., Rosenberg, J., Paz, I., Pupko, T., Fariselli, P., Casadio, R. and Ben-Tal, N. (2004) ConSeq: the identification of functionally and structurally important residues in protein sequences. Bioinformatics 20, 1322-1324 (Pubitemid 38807587)
31. Rahman, M., Ismat, F., McPherson, M. J. and Baldwin, S. A. (2007) Topology-informed strategies for the overexpression and purification of membrane proteins. Mol. Membr. Biol. 24, 407-418 (Pubitemid 47290686)
32. Bernsel, A., Viklund, H., Hennerdal, A. and Elofsson, A. (2009) TOPCONS: consensus prediction of membrane protein topology. Nucleic Acids Res. 37, W465-W468
33. Weeks, D. L. and Sachs, G. (2001) Sites of pH regulation of the urea channel of Helicobacter pylori. Mol. Microbiol. 40, 1249-1259 (Pubitemid 32635296)
34. Weeks, D. L., Gushansky, G., Scott, D. R. and Sachs, G. (2004) Mechanism of proton gating of a urea channel. J. Biol. Chem. 279, 9944-9950 (Pubitemid 38372595)
35. Heuberger, E. H., Veenhoff, L. M., Duurkens, R. H., Friesen, R. H. and Poolman, B. (2002) Oligomeric state of membrane transport proteins analyzed with blue native electrophoresis and analytical ultracentrifugation. J. Mol. Biol. 317, 591-600 (Pubitemid 34722171)
36. Marsh, D. (1999) Quantitation of secondary structure in ATR infrared spectroscopy. Biophys. J. 77, 2630-2637
37. Arrondo, J. L. and Goni, F. M. (1999) Structure and dynamics of membrane proteins as studied by infrared spectroscopy. Prog. Biophys. Mol. Biol. 72, 367-405
38. Bullough, P. A. and Henderson, R. (1990) Phase accuracy in high-resolution electron microscopy of trigonal and orthorhombic purple membrane. Biophys. J. 58, 705-711 (Pubitemid 20312927)
39. Henderson, R. and Unwin, P. N. (1975) Three-dimensional model of purple membrane obtained by electron microscopy. Nature 257, 28-32
40. Chebrou, H., Bigey, F., Arnaud, A. and Galzy, P. (1996) Amide metabolism: a putative ABC transporter in Rhodococcus sp. R312. Gene 182, 215-218 (Pubitemid 27007188)
41. Wilson, S. A., Williams, R. J., Pearl, L. H. and Drew, R. E. (1995) Identification of two new genes in the Pseudomonas aeruginosa amidase operon, encoding an ATPase (AmiB) and a putative integral membrane protein (AmiS). J. Biol. Chem. 270, 18818-18824
42. Bury-Mone, S., Skouloubris, S., Labigne, A. and De Reuse, H. (2001) The Helicobacter pylori UreI protein: role in adaptation to acidity and identification of residues essential for its activity and for acid activation. Mol. Microbiol. 42, 1021-1034 (Pubitemid 33078384)
43. Levin, M. H., de la Fuente, R. and Verkman, A. S. (2007) Urearetics: a small molecule screen yields nanomolar potency inhibitors of urea transporter UT-B. FASEB J. 21, 551-563 (Pubitemid 46213502)